From the Blacktip Shark Carcharhinus Limbatus (Carcharhinidae) in the Northern Gulf of Mexico Stephen A

Home , Sand devil

University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Harold W. Manter Parasitology, Harold W. Manter Laboratory of Laboratory of Parasitology

2-2006 Selachohemecus benzi n. sp. (Digenea: Sanguinicolidae) from the Blacktip Shark Carcharhinus limbatus (Carcharhinidae) in the Northern Gulf of Mexico Stephen A. Bullard Gulf Coast Research Laboratory, [email protected]

Robin M. Overstreet Gulf Coast Research Laboratory, [email protected]

John K. Carlson Southeast Fisheries Science Center, NOAA, [email protected]

Follow this and additional works at: http://digitalcommons.unl.edu/parasitologyfacpubs Part of the Aquaculture and Fisheries Commons, and the Parasitology Commons

Bullard, Stephen A.; Overstreet, Robin M.; and Carlson, John K., "Selachohemecus benzi n. sp. (Digenea: Sanguinicolidae) from the Blacktip Shark Carcharhinus limbatus (Carcharhinidae) in the Northern Gulf of Mexico" (2006). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 898. http://digitalcommons.unl.edu/parasitologyfacpubs/898

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln.

Published in Systematic Parasitology 63:2 (February 2006), pp. 143–154; doi: 10.1007/s11230-005-9010-x Accepted June 6, 2005; published online April 27, 2006. This document is a US government work and is not subject to copyright in the United States.

Selachohemecus benzi n. sp. (Digenea: Sanguinicolidae) from the Blacktip Shark Carcharhinus limbatus (Carcharhinidae) in the Northern Gulf of Mexico

Stephen A. Bullard,1 Robin M. Overstreet,1 and John K. Carlson2

1. Gulf Coast Research Laboratory, Department of Coastal Sciences, University of Southern Mississippi, Ocean Springs, Mississippi, USA 2. Shark Population Assessment Group, National Marine Fisheries Service, Southeast Fisheries Science Center, Panama City, Florida, USA

Corresponding author – Robin M. Overstreet, email [email protected]

Abstract Selachohemecus benzi Bullard & Overstreet n. sp. infects the heart and kidney of the blacktip shark Carcharhinus limbatus in the northern Gulf of Mexico off Florida and Mississippi, USA. Specimens of S. olsoni Short, 1954, the only congener and only other named blood fluke reported from a chondrichthyan in the Gulf of Mexico, were collected from the heart of the Atlantic sharpnose shark Rhizopri- onodon terraenovae from two new localities, Apalachicola Bay, Florida, and Mississippi Sound, Mississippi, USA. The new species differs from S. olsoni by having a larger body (1.4–3.8 mm long), robust tegumental body spines numbering 51–63 along each lateral body margin, a testis extending from the posterior caeca to the ovary, and a medial ovary with lobes. We amend the diagnosis of Selachohemecus Short, 1954 to accommodate it and provide a diagnostic key for all named chondrichthyan blood flukes.

Introduction

Few blood flukes (Sanguinicolidae von Graff, 1907) reportedly infect chondrichthyans (Smith, 1997, 2002). A total of four nominal species, each belonging to monotypic genera, B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006) have been reported from the vascular system of each of two sharks (Short, 1954; Maillard & Ktari, 1978), a ray (Madhavi & Rao, 1970), and two chimaeras (Van der Land, 1967; Kamegai et al., 2002). Only one species, Selachohemecus olsoni Short, 1954, was described previously from a chondrichthyan in the Gulf of Mexico. This study treats a new species of Selachohemecus Short, 1954 from the heart and kidney of a carcharhinid shark from the northern Gulf of Mexico and extends the geographical range of S. olsoni.

Materials and methods

Sharks were captured by gill-net, longline, and hook and line in summer of 1995, 1999, and 2004 as well as by trawl in October 2002 and 2003. Sharks were pithed immediately after capture, and the heart from each shark was extracted, bisected, sprayed with 8.5 ppt so- dium chloride (NaCl) solution or an anticoagulant solution of 5.0 gm NaCl and 2.0 gm NaCl-citrate/L of distilled water to dislodge the flukes, and examined with the aid of a dissecting microscope. Flukes were killed under slight coverslip pressure with heat from an ethanol-burner flame and stored in 5–10% neutral phosphate-buffered formalin. Whole- mounts were stained in Van Cleave’s haematoxylin with several additional drops of Ehr- lich’s haematoxylin, made alkaline at 70% ethanol with lithium carbonate and butyl-amine, dehydrated, cleared in clove oil and mounted in Canada balsam. Several specimens for scanning electron microscopy (SEM) were dehydrated, immersed in hexamethyldisilazane for 15 min, dried under a vacuum for 10 min, and sputter-coated with gold-palladium. Illustrations of mounted specimens were made with the aid of a drawing tube. Measure- ments are reported in micrometers and given as the range followed by the sample size in parentheses. The holotype and two paratypes were deposited in the United States National Parasite Collection (USNPC), and another paratype was deposited in the Natural History Museum, London (NHML).

Selachohemecus Short, 1954

Amended diagnosis Body elongate, 4–10× longer than wide, dorsoventrally flattened, ventrally concave, with posterior end tapering more than anterior end, spined. Tegumental body spines C-shaped, directed ventrally, with each on a separate peduncle, in single ventrolateral column, not continuous posteriorly. Rosethorn-shaped spines lacking. Nervous system with paired lateral nerve cords connecting anteriorly and posteriorly. Mouth medioventral, subterminal. Oral sucker and pharynx lacking. Oesophagus medial, extending posteriorly either straight or sinuously along midline for 1/4–1/3 of body length. Intestine X-shaped, with four short caeca of equal length, lacking diverticula. Testis occupies middle 1/3 of body, posterior to caecal intersection. Auxiliary external seminal vesicle lacking. Cirrus-sac present or absent. Cirrus sinistral, post-gonadal. Ovary considerably post-caecal; post-ovarian space 1/4–1/3 of body length. Laurer’s canal lacking. Oötype dextral, near midline, comprising an inconspicuous ovoid chamber posterior to ovary. Oviducal seminal receptacle present, bulbous or not depending on amount of sperm in duct. Uterus post-gonadal, not extending laterad beyond ventrolateral nerve cords; uterine eggs spheroid, thin-shelled.

2 B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006)

Vitellarium follicular, extending from nerve commissure to ovary, with asymmetrical posterior branches, with longer dextral branch flanking gonads; common collecting duct orig- inating from dextral branch of vitellarium. Common genital pore dorsal, post-gonadal, opening near posterior end of body between midline and sinistral ventrolateral nerve cord. Adults infecting vascular system of carcharhinid sharks. Type-species: S. olsoni Short, 1954 from the heart of Atlantic sharpnose shark Rhizoprionodon terraenovae (Richardson) (as Sco- liodon terranovae) (Carcharhiniformes: Carcharhinidae) from Alligator Harbor, Florida, USA.

Remarks The genera of blood flukes infecting sharks and chimaeras, Selachohemecus Short, 1954, Chi- maerohemecus Van der Land, 1967 and Hyperandrotrema Maillard & Ktari, 1978, differ from all other blood fluke genera by having one or two ventrolateral columns of C-shaped tegumental body spines (Short, 1954; Van der Land, 1967; Maillard & Ktari, 1978). Teleost blood flukes typically have several ventrolateral rows of straight, spike-like tegumental body spines, each with a slightly recurved distal tip, e.g., Elaphrobates euzeti Bullard & Overstreet, 2003 (see Bullard & Overstreet, 2003) and Cardicola spp. (see Bullard & Over- street, 2004). Paradeontacylix McIntosh, 1934, another genus comprised of species that reportedly infect teleosts only, have rosethorn-shaped spines at the posterior body end in addition to spike-like lateral tegumental body spines (McIntosh, 1934; Ogawa & Egusa, 1986). Selachohemecus differs from the other genera of chondrichthyan blood flukes by having an intestine that is X-shaped, consisting of short anterior and posterior caeca of approx- imate equal length, rather than an intestine that is U-shaped, consisting of long posterior caeca only. In addition to that feature, a combination of lacking Laurer’s canal and having a single ventrolateral column of tegumental body spines, a post-caecal ovary and a common genital pore further separates Selachohemecus from the other genera of chondrichthyan blood flukes. Chimaerohemecus has inter-caecal gonads, two ventrolateral columns of tegumental body spines and separate genital pores. Hyperandrotrema has posterior caeca that extend to near the posterior end of the body, a common genital pore and Laurer’s canal present. Orchispirium Madhavi & Rao, 1970, a monotypic genus whose only known species infects the mesenteric vessels of a stingray (Madhavi & Rao, 1970), is unusual because it apparently lacks tegumental body spines and has a testis with 9–11 transverse coils that fill the inter-caecal space.

Selachohemecus benzi n. sp.

Type-host: Carcharhinus limbatus (Valenciennes) blacktip shark (Carcharhiniformes: Carcharhin- idae). Primary site of adult: Attached to luminal surface of atrium and ventricle; other site: kidney (one adult specimen). Type-locality: Northern Gulf of Mexico, Apalachicola Bay, Florida, USA (29°39′N, 85°11′W); other localities: Eastern Gulf of Mexico, Tampa Bay, Florida, USA and Northern Gulf of Mexico, off Mississippi, USA (30°14′N, 88°43′W).

3 B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006)

Prevalence and intensity of infection: 14 of 51 (27%) blacktip sharks off Florida were infected: 6 had 1 worm; 6 had 3–8; and 2 had 15 and 20; 1 of 30 (3%) blacktip sharks from off Missis- sippi and Louisiana was infected with 1 adult specimen. Type-material: Holotype, USNPC (Beltsville, Maryland) No. 95846, Paratypes, USNPC Nos. 95847, 95848; BMNH (London) Reg. No. 2005.6.6.1. Etymology: The name benzi is for Dr. George William Benz (Middle Tennessee State Uni- versity, Murfreesboro, Tennessee, USA) in recognition of his contributions to elasmo- branch parasitology.

Description (Figures 1–25) [Based on 16 whole-mounts, several sputter-coated specimens, and 2 serially sectioned adult specimens.] Body 1,449–3,831 (16) long, 408–597 (16) wide, 3–7× longer than wide (Figure 1). Tegumental body spines 51–63 (16) per side of body or a total of 102–126 (16), ending about 100–208 (8) or 4–7% of body length from posterior end of body; spines in anterior region of body conspicuous; longest spine 20–30 (16) long, 5–12 (16) wide (Figures 3, 12, 14, 15); spines in mid-body and posterior region of body 12–20 (16) long, 5–12 (16) wide (Figures 4–6); base knob-like (Figures 3–6, 15). Peduncles in anterior region of body 30–50 (16) long, 15–37 (16) wide (Figures 12, 15); peduncles in mid-body and posterior region of body 15–30 (13) long, 7–22 (14) wide; peduncular muscle fibers connecting to base of spine. Ventrolateral nerve-cord 1,449–3,831 (15) long, 7–22 (14) wide near midbody at widest level, 77–189 (14) from body margin, confluent in posterior end of body, with secondary branches extending laterally and medially; dorsolateral nerve-cord paired, extending parallel with ventrolateral nerve-cord between that nerve-cord and body margin, c. 5 wide, with secondary branches extending laterally and medially. Primary commissure per- pendicular to midline of body, connecting ventrolateral nerve-cords, 149–263 (13) or 6–10% of body length from anterior end of body, 52–136 (13) across width of worm, 15–32 (13) in diameter; secondary commissures connecting ventrolateral nerve-cords anteriorly and posteriorly; anterior secondary commissure between primary commissure and anterior end of body; posterior secondary commissure just anterior to level of posterior-most lateral tegumental body spines (Figure 1). Sensory papillae abundant in posterior region of body, ventral; some with sensory cilium; sensory cilium 4 long (Figure 13). Mouth 2–5 (10) in diameter, 10–12 (6) from anterior end of body (Figures 1, 2, 12). Oe- sophagus 544–1,105 (14) long or 26–38% of body length, 25–60 (12) in maximum width, ventral to primary nerve-commissure, dorsal to secondary nerve-commissure (Figure 1); oesophageal wall thickening from 1–3 (5) near mouth to 5–22 (5) posteriorly. Oesophageal gland enveloping oesophagus for entire length, with gland-cells most abundant in area 283–472 (5) long or 34–52% of oesophageal length and 50–85 (5) wide or up to 2× width of oesophagus. Caecal intersection 29–31% of body length from anterior end of body; anterior caeca 136–338 (13) long or 7–9% of body length, 17–80 (12) wide; posterior caeca 104–308 (14) long or 6–10% of body length, 10–75 (13) wide, containing granular material within lumen of some individuals (Figure 18); granular material dense, brownish-yellow in stained whole-mounted specimens.

4 B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006)

Figures 1–8. Selachohemecus benzi n. sp. from the heart of the blacktip shark Carcharhinus limbatus. 1. Body of holotype, proximal portion of uterus filled with sperm, ventral view, holotype. 2. Anterior end of different adult showing mouth, flanking tegumental body spines, distal region of oesophagus and scant oesophageal gland-cells abutting oesophagus, ventral view. 3–6. Tegumental body spines. 3. Spine from anterior body region, lateral view; 4. Spines from between caecal intersection and mouth, frontal (at left) and lateral (at right) views; 5. Spine from between genital pore and posterior end of body, lateral view; 6. Spine from near excretory pore, lateral view. 7. Posterior end of body showing excretory bladder and arms, terminal excretory pore and position of posterior- most tegumental body spines, ventral view (nerve not illustrated). 8. Genitalia, oviducal seminal receptacle with sperm, ascending and descending portions of uterus and metraterm with eggs, ventral view. Eggs in the distal portion of the inverted cirrus represent artifact, but their presence demonstrates that eggs can be drawn into this portion of sac. Scale-bars: 1, 500 μm; 2, 150 μm; 3–6, 20 μm; 7, 200 μm; 8, 150 μm. Abbreviations: asnc, anterior secondary nerve commissure; au, ascending uterus; c, cirrus; ca, caecum; cgp, common genital pore; cs, cirrus-sac; du, descending uterus; ea, excretory arms; eb, excretory bladder; ep, excretory pore; m, metraterm; mg, mehlis gland ducts; o, ovary; oe, oesophagus; oo, oötype; osr, oviducal seminal receptacle; pnc, primary nerve commissure; psnc, posterior secondary nerve commissure; sv, seminal vesicle; t, testis; vr, vitelline res- ervoir.

5 B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006)

Figures 9–11. Selachohemecus benzi n. sp. from Carcharhinus limbatus, genitalia of adults demonstrating morphological variability. 9. Ventral view of genitalia (cirrus everted) showing sperm in seminal vesicle, oviducal seminal receptacle and ascending uterus, as well as eggs in the descending uterus and metraterm. 10. Ventral view of genitalia (swol- len cirrus everted) showing obvious cirrus-sac surrounding distal portion of seminal vesicle and no egg in the ascending uterus. 11. Dorsal view of genitalia (cirrus everted) showing constricted proximal portion of seminal vesicle and a few eggs in metraterm. Scale-bars: 150 μm.

Next page Figures 12–19. Selachohemecus benzi n. sp. from Carcharhinus limbatus. 12. Mouth (m) and flanking peduncles and tegumental body spines, ventral view, scanning electron micrograph (SEM). 13. Excretory pore (ep) and sensory papillae, some of which exhibit a cilium (c), ventral view, SEM. 14. Spines and peduncles in anterior region of body, dorsal view, SEM. 15. Dextral anterior-most spine and peduncle with muscle fibers (m) connected to knob-like proximal end of spine, ventral view, light micrograph (LM) of whole-mount. 16. Everted cirrus (ec), lateral view, SEM. 17. Everted cirrus (ec) extruding from common genital pore (cgp), LM of histological section. Note that uterine opening (uo) is just lateral to base of everted cirrus. 18. Granular material (gm) within caecum (ca) near oesophagus (oe), LM of whole-mount. 19. Oötype (oo) and glandular ducts (g) connecting laterally, LM of whole-mount. Scale-bars: 12–14, 20 μm; 15, 10 μm; 16, 100 μm; 17, 50 μm; 18, 100 μm; 19, 15 μm.

6 B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006)

7 B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006)

Figures 20–25. Selachohemecus spp. 20–23. S. benzi n. sp. from Carcharhinus limbatus. 20. Ovary showing central junction of lobes (arrow) that ultimately gives rise to proximal portion of oviduct (not in focal plane), LM of whole-mount. 21. Uterine eggs, LM of whole-mount. 22. Released eggs, same magnification as those of Figure 21, LM of whole- mount. 23. Sperm (s) and ovoid egg (e) associated with common genital pore (cgp), dorsal view, SEM. 24–25. S. olsoni Short, 1954 from the heart of the Atlantic sharpnose shark Rhi- zoprionodon terraenovae. 24. Tegumental body spines from mid-body, SEM, lateral view. 25. Tegumental body spines, two of which are indicated by arrows, from mid-body, lateral view, LM of whole-mount. Scale-bars: 20, 100 μm; 21–23, 10 μm; 24–25, 4 μm.

8 B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006)

Testis 408–1,399 (16) long or 28–40% of body length, 164–442 (16) wide or 40–77% of body width, 2.2–5.7× longer than wide, dorsal to posterior caeca (Figure 1), enclosing rod- like refractive processes; processes extending dorsoventrally, c. 4 in diameter. Post-testicular space 487–1,154 (16) long or 27–35% of body length. Vasa efferentia comprising intercon- necting meshwork of fine ducts entwined throughout testicular tissue, containing sperma- tozoa in all examined specimens, 10–13 (5) in diameter, extending primarily dorsoventrally and along ventral surface of testis, coalescing in posterior region of testis; vas deferens 99– 323 (14) long, 12–45 (14) wide, extends posteriorly along midline and curves slightly sinis- trally before joining cirrus-sac. Cirrus-sac with wall 3–7 (9) thick (Figures 8–11). Seminal vesicle 244–497 (14) long, 30–109 (14) wide, containing sperm in 12 of 16 specimens, runs parallel to sinistral ventrolateral nerve-cord before narrowing and looping dorsally. Cirrus 74–223 (11) long or 26–53% of seminal vesicle length (nonextruded), 25–90 (11) wide or 28– 187% of seminal vesicle width (nonextruded), 87–209 (7) long (extruded) (Figures 8–11, 16, 17). Common genital pore 164–319 (16) or 6–11% of body length from posterior end of body, 62–149 (16) from sinistral body margin, 119–211 (16) from dextral body margin; sperm with cylindrical head and long whip-like tail (Figure 23). Ovary medial, lobed, 109–308 (16) long or 5–9% of body length, 159–452 (16) wide or 37–79% of body width, 110–170% wider than long, occupies space immediately posterior to testis and between ventrolateral nerve-cords, anterior to seminal vesicle and dorsal to vas deferens, contains refractive dorsoventral rod-like processes (Figures 1, 8, 20). Oviduct including oviducal seminal receptacle 99–249 (14) long, 17–37 (14) wide; oviducal seminal receptacle 62–149 (11) long, 20–37 (11) wide. Oötype 17–60 (9) long, 12–30 (9) wide, at level of seminal vesicle (Figures 1, 8–11, 19). Vitellarium with vitelline follicles compacted in dense lobules, occupies space dorsolateral to testis and alimentary tract; common collecting duct 149–348 (11) long, 17–57 (11) wide. Mehlis’ gland comprising a loosely aggregated field of weakly staining cells surrounding lumen of oötype. Uterus extends posteriorly from oötype short distance before curving ventrally and connecting to ascending portion; ascending portion extends anteriorly and diagonally across midline, occasionally filled with eggs (Figure 8) or sperm and thereby superficially resembling seminal vesicle (Fig- ures 9–11), curves ventrally near posterior margin before connecting with descending portion; descending portion extends posteriorly; metraterm weakly muscular, comprising distal-most portion of female reproductive tract, demarcated from descending uterus by obvious constriction (Figures 9–11) or not (Figure 8), with eggs (Figures 8, 9, 11) or not (Figure 10), 119–273 (13) long or 9–29% of uterine length, 15–65 (13) wide, with wall 3–10 (9) thick. Uterine eggs 5–7 (12) in diameter or 5–13% of uterus width at widest level (Figure 21); ejected eggs 11–14 (10) in diameter (presumably much larger when lodged in host tissue [e.g. Bullard & Overstreet, 2003, 2004]), containing 1 large spheroid and darkly staining body as well as several smaller dense lipid-like bodies, with thin shell (Figure 22). Excretory bladder appears c. 70 long, oblong, medial, between posterior confluence of nerve-cord and posterior end of body, with arms; arms c. 5 wide, paired, uniting just anterior to excretory pore, visible in region posterior to genitalia in one specimen; excretory pore medial, terminal, c. 2 wide (Figures 7, 13).

9 B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006)

Discussion

Selachohemecus benzi n. sp. differs most notably from S. olsoni, the only other known species of this genus, by the combination of having a 1.4–3.8 mm long body, robust tegumental body spines numbering 51–63 on each side of the body, a testis extending from the posterior caeca to the ovary, and a medial ovary with lobes. S. olsoni has a smaller body (982– 1,374 × 172–196 lm), minute, sickle-like tegumental body spines numbering 180–310 per each side of the body (Figures 24, 25), a sinistral testis not extending to the posterior caeca, and an ovoid, sinistral ovary overlapping the posterior portion of the testis. We consider S. benzi congeneric with S. olsoni even though S. olsoni apparently lacks a cirrus-sac. We also consider the terminal genitalia in S. olsoni to be a simple version of the more complex genitalia in S. benzi. Based on our interpretation of the genitalia in S. benzi, we consider the structure labeled as the vas deferens by Short (1954) to comprise a seminal vesicle and a short, indistinct cirrus. Furthermore, adults of S. olsoni are minute compared to those of S. benzi, and perhaps components of the genitalia, namely the cirrus-sac, of S. olsoni are difficult to distinguish simply because they are much smaller than those of S. benzi. The single specimen of S. benzi that infected the kidney of a 74 cm TL blacktip shark from Tampa Bay demonstrated that the adult of this species can occur in a site other than the heart. This specimen, not included in the description, was small (1,459 × 309 μm) but had sperm in the seminal vesicle as well as poorly developed eggs (c. 5 μm wide) in the uterus. We did not make detailed live observations of a specimen of S. benzi or S. olsoni, but based on the presence of prominent muscles in each of the lateral peduncles, the tegumental body spines of these sanguinicolids probably pinch host tissue. Upon contracting the peduncular muscle, the flukes may pivot each tegumental body spine at the base, and the distal tip of the spine may arc ventrally and toward the heart tissue (Figure 15). We suspect that the C-shaped tegumental body spines of Hyperandrotrema cetorhini Maillard & Ktari, 1978 and Chimaerohemecus trondheimensis Van der Land, 1967 function similarly. The level of host specificity exhibited by the chondrichthyan blood flukes C. trondheimensis, S. olsoni, S. benzi, Orchispirium heterovitellatum Madhavi & Rao, 1970, and H. cetorhini is indeterminate because the vascular system of few sharks, rays, and chimaeras has been examined critically for the presence of blood flukes (Tables 1, 2). However, based on our limited data, S. olsoni and S. benzi are apparently highly host-specific, each infecting a single host species, even though infected individuals of both shark species were captured simultaneously from Apalachicola Bay, the type-locality for S. benzi. In addition, we examined the hearts of several other shark species from the Northern Gulf of Mexico as well as from Apalachicola Bay, but none was infected (Table 2). We find it particularly noteworthy that an infection was not observed in nine specimens of the spinner shark Carcharhinus brevipinna (Müller & Henle) because it and the blacktip shark are sympatric species that are morphologically similar and closely related (Compagno, 1988).

10 B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006)

Table 1. Sanguinicolids reported from chondrichthyans Parasite Host Site Locality Reference Selachohemecus olsoni Rhizoprionodon terraenovae Atlantic sharpnose heart Alligator Harbor, Florida, USA Short, 1954 shark Apalachicola Bay, Florida, USA Present study Mississippi Sound, Mississippi, USA Present study Selachohemecus benzi n. sp. Carcharhinus limbatus blacktip shark heart Apalachicola Bay, Florida, USA Present study Northern Gulf of Mexico, Present study off Mississippi, USA kidney Tampa Bay, Florida, USA Present study Orchispirium heterovitellatum Himantura imbricata scaly whipray mesenteric vessels Bay of Bengal, Madhavi & Rao, 1970 off Waltair Coast, India

Hyperandrotrema cetorhini1 Cetorhinus maximus basking shark circulatory system Mediterranean Sea, off Tunisia Maillard & Ktari, 1978 not reported Oslofjorden, Norway Smith, 19722 heart North Sea off Montrose, Scotland Smith, 19722 Chimaerohemecus trondheimensis Chimaera monstrosa rabbit fish dorsal aorta Trondheimsfjorden, Norway Van der Land, 1967 not reported Korsfjorden (sic.), Norway Lockyer et al., 2003 Hydrolagus mitsukurii spookfish dorsal aorta and Suruga Bay, Japan Kamegai et al., 2002 postcardinal vein around kidney Chimaerohemecus sp.3 Hydrolagus affinis smalleyed heart North Atlantic Ocean, Karlsbakk et al., 2002 rabbitfish off Southwest Greenland 1. Sproston (1948) stated that, “two specimens only, of a blood fluke belonging to the family Spirorchiidae [sic], were recovered from the branchial blood vessels” of a basking shark caught “just west of Plymouth Sound,” England. These specimens probably are H. cetorhini because this blood fluke infects the basking shark in the region. However, we did not examine Sproston’s (1948) specimens; we do not know where these specimens are now and we do not know of another report that includes a further observation of any of Sproston’s (1948) blood flukes. 2. Bray & Cribb (2003) confirmed the identity of a specimen from Smith’s (1971) collections as H. cetorhini (BMNH 1988.11.24.16). 3. We attempted to borrow these specimens to identify them, but they were no longer in existence.

11 B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006)

Table 2. Sharks examined for blood flukes in the present study Host n Prevalence (%) Locality SQUALIFORMES Dalatiidae – Sleeper sharks Etmopterus gracilispinis broadbanded lanternshark 3 0 Northern Gulf of Mexico Etmopterus hillianus Caribbean lanternshark 1 0 Northern Gulf of Mexico Etmopterus pusillus smooth lanternshark 1 0 Northern Gulf of Mexico Squalus cubensis Cuban dogfish 76 0 Northern Gulf of Mexico SQUATINIFORMES Squatinidae – Angel sharks Squatina dumeril sand devil 27 0 Northern Gulf of Mexico HEXANCHIFORMES Hexanchidae – Cow sharks Heptranchias perlo sharpnose sevengill shark 1 0 Northern Gulf of Mexico CARCHARHINIFORMES Carcharhinidae – Requiem sharks Carcharhinus leucas bull shark 4 0 Northern Gulf of Mexico, off Mississippi Carcharhinus limbatus blacktip shark 17 0 Northern Gulf of Mexico, off Louisiana 13 8 Northern Gulf of Mexico, off Mississippi 15 27 Tampa Bay, Florida 36 28 Northern Gulf of Mexico, off Florida Carcharhinus brevipinna spinner shark 5 0 Northern Gulf of Mexico, off Louisiana 1 0 Northern Gulf of Mexico, off Mississippi 1 0 Northern Gulf of Mexico, off Florida Carcharhinus plumbeus sandbar shark 1 0 Northern Gulf of Mexico Carcharhinus isodon finetooth shark 1 0 Northern Gulf of Mexico, off Louisiana 3 0 Northern Gulf of Mexico, off Florida Carcharhinus acronatus blacknose shark 2 0 Northern Gulf of Mexico, off Mississippi 1 0 Northern Gulf of Mexico, off Florida 5 0 Eastern Gulf of Mexico, off Florida Carcharhinus signatus night shark 1 0 Northern Gulf of Mexico Rhizoprionodon terraenovae Atlantic sharpnose shark 6 33 Northern Gulf of Mexico, off Mississippi 12 17 Northern Gulf of Mexico, off Florida Triakidae – Houndsharks Mustelus canis smooth dogfish 1 0 Northern Gulf of Mexico, off Florida Sphyrinidae – Hammerhead sharks Sphyrna zygaena scalloped hammerhead shark 9 0 Northern Gulf of Mexico, off Florida 1 0 Eastern Gulf of Mexico, off Florida Sphyrna tiburo bonnethead shark 3 0 Eastern Gulf of Mexico, off Florida

12 B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006)

We extend the geographical range of S. olsoni to the northern Gulf of Mexico off Missis- sippi (Tables 1, 2). Previously, S. olsoni was known from off Florida only (Short, 1954). We collected a total of three specimens of S. olsoni from the hearts of two of six Atlantic sharpnose sharks from Mississippi Sound as well as > 20 and > 40 specimens from 2 of 12 Atlantic sharpnose sharks Rhizoprionodon terraenovae from Apalachicola Bay, Florida.

Key to chondrichthyan blood flukes

1. Intestine X-shaped ...... 2 Intestine U-shaped ...... 3 2. Testis entirely post-caecal; ovary sinistral ...... Selachohemecus olsoni Testis ventral to posterior caeca; ovary medial ...... Selachohemecus benzi 3. Testis not coiled ...... 4 Testis coiled ...... Orchispirium heterovitellatum 4. Genital pore common, medial ...... Hyperandrotrema cetorhini Genital pores separate, sinistral ...... Chimaerohemecus trondheimensis

Acknowledgments – We thank R. Palmer (Gulf Coast Research Laboratory [GCRL], The University of Southern Mississippi [USM]) for helping collect the initial specimens of S. benzi in 1995; J. Braswell (INVISTA Incorporated, Dalton Carpet Technology Center, Dalton, Georgia) for help with the scanning electron microscopy; C. Schloss, J. Shaw, and M. Williams (The Gunter Library, GCRL, USM) for bibliographic assistance; J. Brusher, E. Cortes, and D. Bethea (Shark Population Assessment Group, National Oceanic and Atmospheric Administration [NOAA], National Marine Fisheries Ser- vice [NMFS], Panama City, Florida) for helping collect sharks in Apalachicola Bay, Florida, and ad- jacent waters; R. Hueter, M. Henry, and R. Pierce (Mote Marine Laboratory, Sarasota, Florida) for facilitating collections of sharks from Tampa Bay, Florida; J. Petersen, J. Steckler, L. Galle, and N. Jordan (GCRL) for helping collect sharks off Mississippi; M. Grace, W. Ingram, and the officers and crew of the R/V Gordon Gunter and R/V Oregon II (NOAA, NMFS, Pascagoula, Mississippi) for allowing SAB to examine their catch; and G. Benz for helping examine sharks aboard the R/V Gordon Gunter. Grants from the United States Environmental Protection Agency, Gulf of Mexico Program (Award No. MX994732-95-0), National Oceanic and Atmospheric Association (National Marine Fish- eries Service Award NA06FL0501), and a Doctoral Dissertation Improvement Grant from the Na- tional Science Foundation (NSF Award No. 0508856) supported this study.

References

Bray, R. A. & Cribb, T. H. (2003) The digeneans of elasmobranchs—distribution and evolutionary significance. In: Combes, C. & Jourdane, J. (Eds.) Taxonomy, ecology and evolution of metazoan parasites—Livre hommage au Professeur Louis Euzet. Perpignan: Les Presses Universitaires de Perpi- gnan, pp. 67–96. Bullard, S. A. & Overstreet, R. M. (2003) Elaphrobates euzeti gen. and sp. n. (Digenea: Sanguinicolidae) from snappers (Lutjanidae) in the Gulf of Mexico. In: Combes, C. & Jourdane, J. (Eds.) Taxonomy, ecology and evolution of metazoan parasites—Livre hommage au Professeur Louis Euzet. Perpignan: Les Presses Universitaires de Perpignan, pp. 97–113.

13 B ULLARD, O VERSTREET, AND C ARLSON, S YSTEMATIC P ARASITOLOGY 63 (2006)

Bullard, S. A. & Overstreet, R. M. (2004) Two new species of Cardicola (Digenea: Sanguinicolidae) in drums (Sciaenidae) from Mississippi and Louisiana. Journal of Parasitology, 90, 128–136. Compagno, L. J. V. (1988) Sharks of the Order Carcharhiniformes. Princeton, New Jersey: Princeton Uni- versity Press, 486 pp. Kamegai, S., Machida, M. & Kuramochi, T. (2002) Two blood flukes from deep-sea fishes of Suruga Bay, Japan. Bulletin of the National Science Museum Series A (Zoology), 28, 29–34. Karlsbakk, E., Aspholm, P. E., Berg, V., Hareide, N. R. & Berland, B. (2002) Some parasites of the small-eyed rabbitfish, Hydrolagus affinis (Capello, 1867) (Holocephali), caught in the deep waters off SW Greenland. Sarsia, 87, 179–184. Lockyer, A. E., Olson, P. D., Østergaard, P., Rollinson, D., Johnston, D. A., Attwood, S. A., Southgate, V. R., Horak, P., Snyder, S. D., Le, T. H., Agatsuma, T., McManus, D. P., Carmichael, A. C., Naem, S. & Littlewood, D. T. J. (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology, 126, 203–224. Madhavi, R. & Rao, K. H. (1970) Orchispirium heterovitellatum gen. et sp. nov. (Trematoda: Sanguin- icolidae) from the ray fish, Dasyatis imbricatus Day, from Bay of Bengal. Journal of Parasitology, 56, 41–43. Maillard, C. & Ktari, M. H. (1978) Hyperandrotrema cetorhini n. g., n. sp. (Trematoda, Sanguinicolidae) parasite du système circulatoire de Cetorhinus maximus (Selacii). Annales de Parasitologie Humane et Comparée, 53, 359–365. McIntosh, A. (1934) A new blood trematode, Paradeontacylix sanguinicoloides n. g., n. sp., from Seriola lalandi with a key to the species of the family Aporocotylidae. Parasitology, 26, 463–467. Ogawa, K. & Egusa, S. (1986) Two new species of Paradeontacylix McIntosh, 1934 (Trematoda: San- guinicolidae) from the vascular system of a cultured marine fish, Seriola purpurascens. Fish Pathol- ogy, 21, 15–19. Short, R. B. (1954) A new blood fluke, Selachohemecus olsoni, n. g., n. sp. (Aporocotylidae) from the sharp-nosed shark, Scoliodon terra-novae. Proceedings of the Helminthological Society of Washington, 21, 78–82. Smith, J. W. (1972) The blood flukes of cold-blooded vertebrates and some comparison with the schis- tosomes. Helminthological Abstracts, 41, 161–204. Smith, J. W. (1997) The blood flukes (Digenea: Sanguinicolidae and Spirorchidae) of cold-blooded vertebrates: Part 2. Appendix I: Comprehensive parasite-host list; Appendix II: Comprehensive host-parasite list. Helminthological Abstracts, 66, 329–344. Smith, J. W. (2002) Family Sanguinicolidae von Graff, 1907. In: Gibson, D. I., Jones, A. & Bray, R. A. (Eds.) Keys to the Trematoda. Vol. 1. Wallingford: CAB International and The Natural History Mu- seum, pp. 433–452. Sproston, N. G. (1948) On the genus Dinobothrium van Beneden (Cestoda), with a description of two new species from sharks, and a note on Monorygma sp. from the electric ray. Parasitology, 39, 73–90. Van der Land, J. (1967) A new blood fluke (Trematoda) from Chimaera monstrosa L. Proceedings. Kon- inklijke Nederlandse Akademie van Wetenschappen, Section C, Biological and Medical Sciences, 70, 110–120.